Hostname: page-component-78c5997874-j824f Total loading time: 0 Render date: 2024-11-17T14:02:18.276Z Has data issue: false hasContentIssue false
  • English
  • Français

The effect of host age on feeding performance of fleas

Published online by Cambridge University Press:  18 July 2011

VICTORIA LIBERMAN ,
IRINA S. KHOKHLOVA ,
A. ALLAN DEGEN  and
BORIS R. KRASNOV
VICTORIA LIBERMAN
Affiliation:
Mitrani Department of Desert Ecology, Institute for Dryland Environmental Research, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede-Boqer Campus, 84990 Midreshet Ben-Gurion, Israel
IRINA S. KHOKHLOVA
Affiliation:
Wyler Department of Dryland Agriculture, French Associates Institute for Agriculture and Biotechnology of Drylands, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede-Boqer Campus, Midreshet Ben-Gurion, Israel
A. ALLAN DEGEN
Affiliation:
Wyler Department of Dryland Agriculture, French Associates Institute for Agriculture and Biotechnology of Drylands, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede-Boqer Campus, Midreshet Ben-Gurion, Israel
BORIS R. KRASNOV*
Affiliation:
Mitrani Department of Desert Ecology, Institute for Dryland Environmental Research, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede-Boqer Campus, 84990 Midreshet Ben-Gurion, Israel
*
*Corresponding author: Mitrani Department of Desert Ecology, Institute for Dryland Environmental Research, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede-Boqer Campus, 84990 Midreshet Ben-Gurion, Israel. Tel: +972 8 6596841. Fax: +972 8 6596772. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

We asked whether the age of a rodent host affects the feeding performance of fleas. We predicted that fleas would perform better on young and old than on adult rodents. To test this prediction, we determined bloodmeal size, rate of digestion and time of survival after a single bloodmeal in Xenopsylla ramesis feeding on Meriones crassus of different ages. Fleas took less blood from subadult and adult than from juvenile and old animals. Fleas digested blood of old hosts at the highest rate and blood of juvenile hosts most slowly. After a bloodmeal, fleas survived the longest if fed on a juvenile host. The effect of host gender on bloodmeal size and survival after a bloodmeal was manifested only in (a) subadult and adult hosts and (b) subadult hosts, respectively. Host gender affected the rate of digestion differently among digestion stages and host age cohorts. We explain the observed patterns in flea performance in terms of changes in the host's immune defences and nutritional quality of blood during the host's individual life. Our observations suggested that a host of a particular age could not be unequivocally predicted to be more or less beneficial for a parasite than a younger or an older host.

Keywords

bloodmeal sizedigestionfleasrodents
Type
Research Article
Information
Parasitology , Volume 138 , Issue 9 , August 2011 , pp. 1154 - 1163
Copyright
Copyright © Cambridge University Press 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Arlt, W. and Hewison, M. (2004). Hormones and immune function: implications of aging. Aging Cell 3, 209–216.CrossRefGoogle ScholarPubMed
Carlier, Y. and Truyens, C. (1995). Influence of maternal infection on offspring resistance towards parasites. Parasitology Today 11, 94–99.CrossRefGoogle ScholarPubMed
Castro, J. M., Nolan, V. and Ketterson, E. D. (2001). Steroid hormones and immune function: experimental studies in wild and captive dark-eyed juncos (Junco hyemalis). American Naturalist 157, 408–420.CrossRefGoogle Scholar
Combes, C. (2001). Parasitism. The Ecology and Evolution of Intimate Interactions. University of Chicago Press, Chicago, IL, USA.Google Scholar
Dewar, A. L., Doherty, K. V., Woods, G. M., Lyons, B. L. and Muller, H. K. (2001). Acquisition of immune function during the development of the Langerhans cell network in neonatal mice. Immunology 103, 61–69.CrossRefGoogle ScholarPubMed
Fichet-Calvet, E., Wang, J., Jomaa, I., Ben Ismail, R. and Ashford, R. W. (2003). Patterns of the tapeworm Raillietina trapezoides infection in the fat sand rat Psammomys obesus in Tunisia: season, climatic conditions, host age and crowding effects. Parasitology 126, 481–492.CrossRefGoogle ScholarPubMed
Goater, C. P. and Ward, P. I. (1992). Negative effects of Rhabdias bufonis (Nematoda) on the growth and survival of toads (Bufo bufo). Oecologia 89, 161–165.CrossRefGoogle ScholarPubMed
Gregory, R. D., Montgomery, S. S. J. and Montgomery, W. I. (1992). Population biology of Heligmosomoides polygyris (Nematoda) in the wood mouse. Journal of Animal Ecology 61, 749–757.CrossRefGoogle Scholar
Grenfell, B. T., Dietz, K. and Roberts, M. G. (1995). Modelling the immuno-epidemiology of macroparasites in naturally-fluctuated host populations. In Ecology of Infectious Diseases in Natural Populations (ed. Grenfell, B. T. and Dobson, A. P.), pp. 362–383. Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
Gryseels, B. (1994). Human resistance to Schistosoma infections: age or experience? Parasitology Today 10, 380–384.CrossRefGoogle ScholarPubMed
Gruver, A. L., Hudson, L. L. and Sempowski, G. D. (2007). Immunosenescence of ageing. Journal of Pathology 211, 144–156.CrossRefGoogle ScholarPubMed
Hasselquist, D. and Nilsson, J.-A. (2009). Maternal transfer of antibodies in vertebrates: trans-generational effects on offspring immunity. Philosophical Transactions of the Royal Society B 364, 51–60.CrossRefGoogle ScholarPubMed
Hawlena, H., Abramsky, Z. and Krasnov, B. R. (2005). Age-biased parasitism and density-dependent distribution of fleas (Siphonaptera) on a desert rodent. Oecologia 146, 200–208.CrossRefGoogle ScholarPubMed
Hawlena, H., Krasnov, B. R., Abramsky, Z., Khokhlova, I. S., Gouey de Bellocq, J. and Pinshow, B. (2008). Effects of food abundance, host age, and flea infestation on the body condition and immunological variables of a rodent host, and their consequences for parasite survival. Comparative Biochemistry and Physiology A 150, 66–74.CrossRefGoogle Scholar
Henricson, J. (1977). The abundance and distribution of Diphyllobothrium dendriticum (Nitzsch) and D. ditrenum (Creplin) in the char Salvelinus alpinus. Journal of Fish Biology 11, 231–248.CrossRefGoogle Scholar
Hudson, P. J. and Dobson, A. P. (1995). Macroparasites: Observed patterns. In Ecology of Infectious Diseases in Natural Populations (ed. Grenfell, B. T. and Dobson, A. P.), pp. 144–176. Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
Ioff, I. G. (1941). Ecology of Fleas in Relevance to Their Medical Importance. Pyatygorsk Publishers, Pyatygorsk, USSR (in Russian).Google Scholar
Khokhlova, I. S., Ghazaryan, L., Krasnov, B. R. and Degen, A. A. (2008). Effects of parasite specificity and previous infestation of hosts on the feeding and reproductive success of rodent-infesting fleas. Functional Ecology 22, 530–536.CrossRefGoogle Scholar
Khokhlova, I. S., Kam, M., Gonen, S. and Degen, A. A. (2000). Level of energy intake affects the estrous-cycle in Sundevall's jird (Meriones crassus). Physiological and Biochemical Zoology 73, 257–263.CrossRefGoogle ScholarPubMed
Khokhlova, I. S., Serobyan, V., Krasnov, B. R. and Degen, A. A. (2009 a). Effect of host gender on blood digestion in fleas: mediating role of environment. Parasitology Research 105, 1667–1673.CrossRefGoogle ScholarPubMed
Khokhlova, I. S., Serobyan, V., Krasnov, B. R. and Degen, A. A. (2009 b). Is the feeding and reproductive performance of the flea, Xenopsylla ramesis, affected by the gender of its rodent host, Meriones crassus? Journal of Experimental Biology 212, 1429–1435.CrossRefGoogle ScholarPubMed
Khokhlova, I. S., Serobyan, V., Degen, A. A. and Krasnov, B. R. (2010). Host gender and offspring quality in a flea parasitic on a rodent. Journal of Experimental Biology 213, 3299–3304.CrossRefGoogle Scholar
Khokhlova, I. S., Spinu, M., Krasnov, B. R. and Degen, A. A. (2004). Immune response to fleas in a wild desert rodent: Effect of parasite species, parasite burden, sex of host and host parasitological experience. Journal of Experimental Biology 207, 2725–2733.CrossRefGoogle Scholar
Klein, S. L. (2004). Hormonal and immunological mechanisms mediating sex differences in parasite infection. Parasite Immunology 26, 247–264.CrossRefGoogle ScholarPubMed
Knopf, P. M. and Coghlan, R. L. (1989). Maternal transfer of resistance to Schistosoma mansoni. Journal of Parasitology 75, 398–404.CrossRefGoogle ScholarPubMed
Krasnov, B. R. (2008). Functional and Evolutionary Ecology of Fleas: a Model for Ecological Parasitology. Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
Krasnov, B. R., Burdelova, N. V., Shenbrot, G. I. and Khokhlova, I. S. (2002 b). Annual cycles of four flea species (Siphonaptera) in the central Negev desert. Medical and Veterinary Entomology 16, 266–276.CrossRefGoogle ScholarPubMed
Krasnov, B. R., Khokhlova, I. S., Burdelova, N. V., Mirzoyan, N. S. and Degen, A. A. (2004). Fitness consequences of density-dependent host selection in ectoparasites: testing reproductive patterns predicted by isodar theory in fleas parasitizing rodents. Journal of Animal Ecology 73, 815–820.CrossRefGoogle Scholar
Krasnov, B. R., Khokhlova, I. S., Fielden, L. J. and Burdelova, N. V. (2002 a). Time to survival under starvation in two flea species (Siphonaptera: Pulicidae) at different air temperatures and relative humidities. Journal of Vector Ecology 27, 70–81.Google ScholarPubMed
Krasnov, B. R. and Matthee, S. (2010). Spatial variation in gender-biased parasitism: host-related, parasite-related and environment-related effects. Parasitology 137, 1526–1537.CrossRefGoogle ScholarPubMed
Krasnov, B. R., Morand, S., Hawlena, H., Khokhlova, I. S. and Shenbrot, G. I. (2005). Sex-biased parasitism, seasonality and sexual size dimorphism in desert rodents. Oecologia 146, 209–217.CrossRefGoogle ScholarPubMed
Krasnov, B. R., Sarfati, M., Arakelyan, M. S., Khokhlova, I. S., Burdelova, N. V. and Degen, A. A. (2003). Host-specificity and foraging efficiency in blood-sucking parasite: feeding patterns of a flea Parapulex chephrenis on two species of desert rodents. Parasitology Research 90, 393–399.CrossRefGoogle ScholarPubMed
Krasnov, B. R., Shenbrot, G. I., Medvedev, S. G., Vatshenok, V. S. and Khokhlova, I. S. (1997). Host-habitat relations as an important determinant of flea assemblages (Siphonaptera) on rodents in the Negev Desert. Parasitology 114, 159–173.CrossRefGoogle ScholarPubMed
Krasnov, B. R., Stanko, M. and Morand, S. (2006). Age-dependent flea (Siphonaptera) parasitism in rodents: a host's life history matters. Journal of Parasitology 92, 242–248.CrossRefGoogle ScholarPubMed
Møller, A. P. and de Lope, F. (1999). Senescence in a short-lived migratory bird: age-dependent morphology, migration, reproduction and parasitism. Journal of Animal Ecology 68, 163–171.CrossRefGoogle Scholar
Pacala, S. W. and Dobson, A. P. (1988). The relation between the number of parasites/host and host age: population dynamic causes and maximum likelihood estimation. Parasitology 96, 197–210.CrossRefGoogle ScholarPubMed
Rolff, J. (2002). Bateman's principle and immunity. Proceedings of the Royal Society of London, B 269, 867–872.CrossRefGoogle ScholarPubMed
Rousset, F., Thomas, F., de Meeûs, T. and Renaud, F. (1996). Inference of parasite-induced host mortality from distribution of parasite loads. Ecology 77, 2203–2211.CrossRefGoogle Scholar
Sarfati, M., Krasnov, B. R., Ghazaryan, L., Khokhlova, I. S., Fielden, L. J. and Degen, A. A. (2005). Energy costs of blood digestion in a host-specific haematophagous parasite. Journal of Experimental Biology 208, 2489–2496.CrossRefGoogle Scholar
Shelley, J. B. and Juhlin, L. (1976). Langerhans cells form a reticuloepithelial trap for external contact sensitizers. Nature, London 261, 46.CrossRefGoogle Scholar
Vashchenok, V. S. (1988). Fleas – Vectors of Pathogens Causing Diseases in Humans and Animals. Nauka, Leningrad, USSR (in Russian).Google Scholar
Vashchenok, V. S. and Solina, L. T. (1969). On blood digestion in fleas Xenopsylla cheopis Roths. (Aphaniptera, Pulicidae). Parazitologiya 3, 451–460 (in Russian).Google Scholar
Woolhouse, M. J. E. (1998). Patterns in parasite epidemiology: the peak shift. Parasitology Today 14, 428–434.CrossRefGoogle ScholarPubMed
Zuk, M. (1996). Disease, endocrine-immune interactions, and sexual selection. Ecology 77, 1037–1042.CrossRefGoogle Scholar